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Catalase in Brachionus Calyciflorus During the Aging Process Changes in Expression of Manganese Superoxide Dismutase, Copper and Zinc Superoxide Dismutase and Catalase in Brachionus calyciflorus during the Aging Process Jianghua Yang, Siming Dong, Qichen Jiang, Tengjiao Kuang, Wenting Huang, Jiaxin Yang* Jiangsu Province Key Laboratory for Biodiversity & Biotechnology and Jiangsu Province Key Laboratory for Aquatic Live Food, School of Biological Sciences, Nanjing Normal University, Nanjing, Jiangsu, People’s Republic of China Abstract Rotifers are useful model organisms for aging research, owing to their small body size (0.1–1 mm), short lifespan (6–14 days) and the relative easy in which aging and senescence phenotypes can be measured. Recent studies have shown that antioxidants can extend the lifespan of rotifers. In this paper, we analyzed changes in the mRNA expression level of genes encoding the antioxidants manganese superoxide dismutase (MnSOD), copper and zinc SOD (CuZnSOD) and catalase (CAT) during rotifer aging to clarify the function of these enzymes in this process. We also investigated the effects of common life- prolonging methods [dietary restriction (DR) and resveratrol] on the mRNA expression level of these genes. The results showed that the mRNA expression level of MnSOD decreased with aging, whereas that of CuZnSOD increased. The mRNA expression of CAT did not change significantly. This suggests that the ability to eliminate reactive oxygen species (ROS) in the mitochondria reduces with aging, thus aggravating the damaging effect of ROS on the mitochondria. DR significantly increased the mRNA expression level of MnSOD, CuZnSOD and CAT, which might explain why DR is able to extend rotifer lifespan. Although resveratrol also increased the mRNA expression level of MnSOD, it had significant inhibitory effects on the mRNA expression of CuZnSOD and CAT. In short, mRNA expression levels of CAT, MnSOD and CuZnSOD are likely to reflect the ability of mitochondria to eliminate ROS and delay the aging process. Citation: Yang J, Dong S, Jiang Q, Kuang T, Huang W, et al. (2013) Changes in Expression of Manganese Superoxide Dismutase, Copper and Zinc Superoxide Dismutase and Catalase in Brachionus calyciflorus during the Aging Process. PLoS ONE 8(2): e57186. doi:10.1371/journal.pone.0057186 Editor: Gabriele Sorci, CNRS, Universite´ de Bourgogne, France Received November 5, 2012; Accepted January 18, 2013; Published February 22, 2013 Copyright: ß 2013 Yang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the National Natural Science Foundation of China (No.: 31272388) to JXY and National Natural Science Foundation of China for Talents Training in Basic Science (J1103507). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction in rotifer aging. However, there are few reports of changes during aging in the expression of genes encoding antioxidant enzymes. Reactive oxygen species (ROS), such as hydrogen peroxide 2 The rotifer Brachionus calyciflorus has a short lifespan (5–7 days) and (H2O2) and superoxide anion (O2 ), are produced mainly as by- it is easy to detect changes in gene expression during the aging products of aerobic respiration and can damage many cell process in this species. Therefore, we analyzed changes in the macromolecules, including lipids, proteins and nucleic acids [1]. mRNA expression level of genes encoding the antioxidants This damage has been hypothesized to be the major contributor to manganese SOD (MnSOD) [14], copper and zinc SOD the aging process [1–4]. However, organisms have well-developed (CuZnSOD) and CAT (GenBank accession no. JX000005, defense systems to eliminate ROS [5]. For example, antioxidant JX515577 and JX515578, respectively) in B. calyciflorus individuals enzymes, such as superoxide dismutase (SOD) and catalase (CAT), of different ages to explore the role of such enzymes in the aging catalyze the decomposition of ROS [6,7], thereby moderating process. oxidative stresses and resulting in longer lifespan [8]. Previous Dietary restriction (DR) is usually defined as a moderate studies have shown that SOD expression enhancement can extend (normally 20–40%) reduction of available nutrients without the lifespan of the nematode Caenorhabditis elegans [9] and the fruit causing malnutrition. It was first noted during the 1930s that fly Drosophila melanogaster [10]. Rotifers are important members of DR significantly extended the lifespan of rodents [15]. In the freshwater zooplankton communities and, because of their laboratory, DR is one of the most commonly used life-history ecological significance, are increasingly being used in ecotoxico- alterations among evolutionarily distinct eukaryotes, from single- logical studies [11,12]. In addition, they are often used in aging cell to multicellular organisms [16–19]. Previous studies have research, because of their small body size (0.1–1 mm in length) suggested that DR can extend the lifespan of rotifers and enhance and short lifespan (6–14 days). Studies have also shown that their resistance to oxidative stress [20–24]. Interestingly, DR- antioxidants can extend the rotifer lifespan [13], which suggests induced longevity and other beneficial effects of DR can transmit that genes encoding antioxidant enzymes have an important role PLOS ONE | www.plosone.org 1 February 2013 | Volume 8 | Issue 2 | e57186 Antioxidant Enzyme Contribute to Delaying Aging to the next generation in rotifers [25]. Resveratrol (3,5,40- Dietary restriction. Rotifers hatched from resting eggs were trihydroxy-trans-stilbene) is a polyphenolic phytoallexin found in cultured for 24 h in normal media. In total, 100 rotifers were then a variety of plant products [26], and has been reported to have selected at random and transferred into 50 mL of DR medium (i.e. beneficial effects on lifespan in many organisms, including yeast no food) and starved for 12, 24 and 48 h. As above, each Saccharomyces cerevisiae [26], D. melanogaster, C. elegans [27,28] and the treatment had three replicates. Rotifers were transferred into fish Nothobranchius furzeri [29]. It also has been reported that newly prepared culture media every 24 h and checked every 12 h resveratrol can protect against ROS-induced cell death by to remove neonates. Rotifers were collected at 12, 24 and 48 h and inhibiting ROS formation [30], preventing mitochondrial dys- the total RNA was then extracted. function [31] and restoring SOD activity [32]. Oxidative stress resistance in rotifers pretreated with DR The objective of present study was to investigate the effects of or resveratrol. Rotifers hatched from resting eggs were DR and resveratrol on the expression levels of the genes encoding pretreated by either DR (i.e. provided with food once every MnSOD, CuZnSOD and CAT. Lifespan extension is always 12 h) or resveratrol (5 mM), and were then transferred into accompanied by an increase in viability in wide variety of species. paraquat (15.25 mg/L) media. Ten rotifers were added to six-well Therefore we exposed the rotifers pretreated with DR and culture plates that contained 5 mL of the test solution. Each resveratrol to oxidative stress, and analyzed their survival. treatment had three replicates. The number of rotifers surviving after 12 h and 24 h was recorded. Resveratrol was dissolved in Materials and Methods acetone and stored at 220uC. Paraquat (DMSO stock) was obtained from the Jiangsu Academy of Agricultural Sciences Rotifers (Nanjing, China). The animals used during the study, Brachionus calyciflorus (Pallas), Age-related changes in swimming speed. To measure the were neonate females (0–2-h old) hatched from resting eggs in rotifer swimming speed, we modified the method of Snell et al. artificial freshwater medium (EPA medium, pH ,7.8) that (2011) as follows [13]. Experiments were carried out in a 48-well comprised 96 mg NaHCO3, 60 mg CaSO4?H2O, 123 mg plate (10.20 mm in diameter) that contained 100 mL EPA. Video MgSO4, and 4 mg KCl in 1 L deionized water at 25uC [33]. footage of rotifers swimming at 64 magnification was captured Members of this species were originally collected in Gainesville, with a camera attached to a LEICA EZ4D stereomicroscope. Florida in 1983 [34] and, since then, have been cultured AutoCAD 2011 software was used to estimate the swimming speed continuously in the laboratory with periodic collection and storage (mm/s) of individual rotifers. From each age groups (0, 1, 2, 3, 4 of resting eggs. The females were fed by suspending the green alga and 5 days), eight to ten randomly selected rotifers were each Chlorella pyrenoidosa (Institute of Hydrobiology, Chinese Academy of videoed swimming for at least 1 min to measure the swimming 6 Sciences, Wuhan, China) in the culture media at ,3610 cells per speed. mL. The feeding alga was cultured in BBM (Bolds Basal Medium) Quantitative analysis of gene transcription. Total RNAs medium at 25uC in 3 L flasks under constant fluorescent were extracted using the procedures described above. Total RNA illumination at 2000 lux. was reverse-transcribed into cDNA using the PrimeScript RT Reagent Kit (TaKaRa, Japan). Real-time PCR was performed on Experimental design a Mastercycler Ep Realplex (Eppendorf, Germany) to study the Age-related changes in antioxidant enzyme gene gene expression. The PCR reaction was performed in a 25 mL expression. In total, 600 neonates (0–2-h old) were collected volume with a SYBR Premix Ex TaqTMKit (TaKaRa, Japan), and divided into six groups of 100 individuals, which were then 2 mM of each specific primer, and 1 mL of cDNA using the cultured in 50 mL of prepared media maintained at 25uC for 0.5, following procedure: initial denaturation at 95uC for 2 min 1, 2, 3, 4 and 5 days. Each treatment had three replicates.
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